Putrescine Is an Intraspecies and Interkingdom Cell-Cell Communication Signal Modulating the Virulence of Dickeya zeae

Shi, Zurong; Wang, Qingwei; Li, Yasheng; Liang, Ziwen; Xu, Luzhou; Zhou, Jianuan; Cui, Zi‐Ning; Zhang, Lian-Hui

doi:10.3389/fmicb.2019.01950

Cited by 43 publications

(71 citation statements)

References 47 publications

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“…4 ). This is similar to our recent findings in which blocking putrescine signaling did not affect zeamine production in D. zeae EC1 but led to decreased bacterial swimming motility and an attenuated invasion capability ( 18 ). We also found that the nonmotile Δ fliG mutant significantly decreased the colonization and inhibition ability, which was comparable to the 7PDE strain ( Fig.…”

Section: Discussionsupporting

confidence: 92%

“…Furthermore, several regulatory mechanisms associated with c-di-GMP turnover have been implicated in D. zeae virulence from our previous findings; specifically, the two-component system proteins VfmIH and a global transcriptional regulator, SlyA, were reported to regulate some key c-di-GMP turnover enzymes at the transcriptional level, including the primary DGC14945 enzyme ( 14 , 16 ). The AHL quorum sensing signal as well as host-pathogen communication through putrescine signaling were reported to mainly regulate flagellar motility and biofilm formation ( 17 , 18 ). Given that the overlap between c-di-GMP and other regulatory systems is widespread within numerous bacterial species, it would be interesting to investigate the connection between c-di-GMP and these systems.…”

Section: Discussionmentioning

confidence: 99%

“…In addition, several regulatory mechanisms associated with D. zeae virulence have been uncovered in recent years, including the transcription factors SlyA and Fis ( 14 , 15 ); a two-component regulatory system, VfmHI ( 16 ); an acyl-homoserine lactone (AHL)-mediated quorum sensing (QS) system ( 17 ); a polyamine-mediated host-pathogen communication system ( 18 ); and the bacterial second messenger cyclic di-GMP (c-di-GMP) ( 19 ). These findings present both a framework and useful clues for dissecting the molecular mechanisms and signaling networks by which D. zeae modulates its physiology and virulence.…”

Section: Introductionmentioning

confidence: 99%

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Systematic Analysis of c-di-GMP Signaling Mechanisms and Biological Functions in Dickeya zeae EC1

Chen

Zhou

et al. 2020

mBio

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Dickeya zeae is an important and aggressive bacterial phytopathogen that can cause substantial economic losses in banana and rice plantations. We previously showed that c-di-GMP signaling proteins (cyclases/phosphodiesterases) in D. zeae strain EC1 play a significant role in the bacterial sessile-to-motile transition. To determine whether there is any synergistic effect among these c-di-GMP signaling proteins, we prepared a series of mutant strains by generating consecutive in-frame deletions of the genes encoding diguanylate cyclases (which make c-di-GMP) and phosphodiesterases (which break down c-di-GMP), respectively, using EC1 as a parental strain. The results showed that the complete deletion of all the putative diguanylate cyclases resulted in significantly increased bacterial motility and abrogated biofilm formation but did not appear to affect pathogenicity and virulence factor production. In contrast, the deletion of all the c-di-GMP phosphodiesterase genes disabled motility and prevented the invasion of EC1 into rice seeds. By measuring the c-di-GMP concentrations and swimming motility of all the mutants, we propose that c-di-GMP controlled swimming behavior through a multitiered program in a c-di-GMP concentration-dependent manner, which could be described as an L-shaped regression curve. These features are quite different from those that have been shown for other bacterial species such as Salmonella and Caulobacter crescentus. Further analysis identified three c-di-GMP signaling proteins, i.e., PDE10355, DGC14945, and PDE14950, that play dominant roles in influencing the global c-di-GMP pool of strain EC1. The findings from this study highlight the complexity and plasticity of c-di-GMP regulatory circuits in different bacterial species. IMPORTANCE Dickeya zeae is the etiological agent of bacterial foot rot disease, which can cause massive economic losses in banana and rice plantations. Genome sequence analysis showed that D. zeae strain EC1 contains multiple c-di-GMP turnover genes, but their roles and regulatory mechanisms in bacterial physiology and virulence remain vague. By generating consecutive in-frame deletion mutants of the genes encoding c-di-GMP biosynthesis and degradation, respectively, we analyzed the individual and collective impacts of these c-di-GMP metabolic genes on the c-di-GMP global pool, bacterial physiology, and virulence. The significance of our study is in identifying the mechanism of c-di-GMP signaling in strain EC1 more clearly, which expands the c-di-GMP regulating patterns in Gram-negative species. The methods and experimental designs in this research will provide a valuable reference for the exploration of the complex c-di-GMP regulation mechanisms in other bacteria.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Systematic Analysis of c-di-GMP Signaling Mechanisms and Biological Functions in Dickeya zeae EC1

Chen

Zhou

et al. 2020

mBio

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“…Among them were ter operon coding for tellurite resistance genes [43], potABC involved in spermidine/putrescine polyamine uptake [44], kdpBCDE coding for two-component regulators and ATPases involved in potassium uptake [45] and pectin lyase pnlA gene activated during UV stress and cell lysis [46]. Pectin lyase production [47] and potassium [48] and putrescine uptake [49] have been linked previously to virulence or cell-cell communication in soft rot bacteria. In addition, P. parvum lacked several small operons coding for PTS transporters with adjacent aldolase or sugar kinase, suggesting that P. parvum may not be able to fully utilize all sugars and polysaccharides present in plant tissues.…”

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confidence: 99%

Pectobacterium parvum sp. nov., having a Salmonella SPI-1-like Type III secretion system and low virulence

Pasanen

Waleron

Schott

et al. 2020

International Journal of Systematic and Evolutionary Microbiology

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Pectobacterium strains isolated from potato stems in Finland, Poland and the Netherlands were subjected to polyphasic analyses to characterize their genomic and phenotypic features. Phylogenetic analysis based on 382 core proteins showed that the isolates clustered closest to Pectobacterium polaris but could be divided into two clades. Average nucleotide identity (ANI) analysis revealed that the isolates in one of the clades included the P. polaris type strain, whereas the second clade was at the border of the species P. polaris with a 96 % ANI value. In silico genome-to-genome comparisons between the isolates revealed values below 70%, patristic distances based on 1294 core proteins were at the level observed between closely related Pectobacterium species, and the two groups of bacteria differed in genome size, G+C content and results of amplified fragment length polymorphism and Biolog analyses. Comparisons between the genomes revealed that the isolates of the atypical group contained SPI-1-type Type III secretion island and genes coding for proteins known for toxic effects on nematodes or insects, and lacked many genes coding for previously characterized virulence determinants affecting rotting of plant tissue by soft rot bacteria. Furthermore, the atypical isolates could be differentiated from P. polaris by their low virulence, production of antibacterial metabolites and a citrate-negative phenotype. Based on the results of a polyphasic approach including genome-to-genome comparisons, biochemical and virulence assays, presented in this report, we propose delineation of the atypical isolates as a novel species Pectobacterium parvum, for which the isolate s0421 T (CFBP 8630 T =LMG 30828 T) is suggested as a type strain.

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“…Moreover, polyamines such as spermidine and spermine are reported to be involved in the interkingdom communications, which are transported into the cell through ABC transporter SpuBCDEF and further activate expression of the genes involved in the T3SS in P. aeruginosa (Shi et al., 2019) through which bacteria may consequently acquire antibiotic resistance. Thus, it would be an interesting field to explore the role of polyamines as a QS molecule.…”

Section: Discussionmentioning

confidence: 99%

Polyamines in the virulence of bacterial pathogens of respiratory tract

Banerji

Kanojiya

Patil

et al. 2020

Molecular Oral Microbiology

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Polyamines are positively charged hydrocarbons that are essential for the growth and cellular maintenance in prokaryotes and eukaryotes. Polyamines have been demonstrated to play a role in bacterial pathogenicity and biofilm formation. However, the role of extracellular polyamines as a signaling molecule in the regulation of virulence is not investigated in detail. The bacterial pathogens residing in the respiratory tract remain asymptomatic for an extended period; however, the factors that lead to symptomatic behavior are poorly understood. Further investigation to understand the relation between the host‐secreted factors and virulence of pathogenic bacteria in the respiratory tract may provide insights into the pathogenesis of respiratory tract infections. Polyamines produced within the bacterial cell are generally sequestered. Therefore, the pool of extracellular polyamines formed by secretion of the commensals and the host may be one of the signaling molecules that might contribute toward the alterations in the expression of virulence factors in bacterial pathogens. Besides, convergent mechanisms of polyamine biosynthesis do exist across the border of species and genus level. Also, several novel polyamine transporters in the host and bacteria remain yet to be identified. The review focuses on the role of polyamines in the expression of virulence phenotypes and biofilm formation of the respiratory tract pathogens.

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Putrescine Is an Intraspecies and Interkingdom Cell-Cell Communication Signal Modulating the Virulence of Dickeya zeae

Cited by 43 publications

References 47 publications

Systematic Analysis of c-di-GMP Signaling Mechanisms and Biological Functions in Dickeya zeae EC1

Systematic Analysis of c-di-GMP Signaling Mechanisms and Biological Functions in Dickeya zeae EC1

Pectobacterium parvum sp. nov., having a Salmonella SPI-1-like Type III secretion system and low virulence

Polyamines in the virulence of bacterial pathogens of respiratory tract

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